FORKTAIL 32 (2016): 72–85

The birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines, including accounts of breeding seabird population trends ARNE E. JENSEN & ANGELIQUE SONGCO

Data on the seabird population of Tubbataha Reefs Natural Park, Palawan province, Philippines, which lies in the Sulu Sea, date back to 1911. However, regular surveys and monitoring began only in 1997 and have resulted in a wealth of new information. An annotated list of the 106 recorded species is presented and changes in the population of the seven breeding seabird species and the factors that influence such changes are discussed. From an estimated 13,500 breeding seabirds in 1981, the population decreased to less than a third of that number in 2003, with the only Philippine population of Masked Booby Sula dactylatra being extirpated in 1995. Thanks to strict enforcement of a no-visitor policy from 1997, the population increased to around 32,300 birds in 2013. The park is the only known breeding area of the subspecies worcesteri of Black Noddy Anous minutus. It hosts the largest breeding colonies of Brown Booby Sula leucogaster, Greater Crested Tern Thalasseus bergii and Brown Noddy A. stolidus, and the second-largest populations of Red-footed Booby Sula sula and Sooty Tern Onychoprion fuscatus, in the Philippine archipelago. Data on other breeding sites of these species in the archipelago are included. Two new species for the Philippines, 14 new species for Palawan province and four globally threatened species, including the Critically Endangered Christmas Frigatebird Fregata andrewsi, together with first Philippine records of Yellow Wagtail Motacilla flava tschutschensis and M. f. macronyx are described. Since 1981 there has been a reduction in land area of over 40%, but the previously barren islets are now vegetated and this has encouraged expansion of tree-nesting Red-footed Booby and Black Noddy colonies to the detriment of Brown Booby. Temperature anomalies caused by El Niño and La Niña events appear to affect the breeding cycle of seabirds.

INTRODUCTION provinces and other countries, together with the introduction of cyanide and dynamite "shing techniques. Commercial scuba !e uninhabited Tubbataha Reefs Natural Park lies in the Sulu diving started in 1979 and within a few years the remote reefs were Sea, 170 km south-east of Puerto Princesa City, Palawan province, transformed into a priority destination for local and international Philippines. !e area was designated a protected national marine scuba divers (Arquiza & White 1999, Songco 2003, Dygico 2006). park in 1988 and as a natural marine park in 2006. !e protected Today the dive season is restricted to three months (mid-March to area was expanded to include the Jessie Beazley Reef in 2010. It was mid-June), whilst permits and entrance fees provide the necessary declared a UNESCO World Heritage Site in 1993 and in 1999 was funds to manage and patrol the park. included in the Ramsar list of Wetlands of International Importance (Ramsar 2016, UNESCO 2016). There have been few studies of birds in the Sulu Sea and STUDY AREA published data on the avifauna of the atolls and islets are largely based on the collection of specimen or sight records from a century The 97,000 ha Tubbataha Reefs Natural Park, lying between ago. Early collectors included Richard McGregor in January 1903 8.761°N 119.844°E and 9.052°N 119.817°E, includes the North and Dean Worcester, who visited the Tubbataha Reefs in June 1911 and South Atolls and the Jessie Beazley Reef (Figure 1). !e total and provided the "rst description of its seabird colony (McGregor exposed area of these formations at high tide is about 14,000 m$. 1904, Worcester 1911). No further ornithological surveys were Bird Islet, previously known as North Islet (Plate 1), located undertaken in this area until a survey by the Haribon Foundation in the North Atoll (8.931°N 119.997°E), had a circumference of for Conservation of Natural Resources in 1981 (Kennedy 1982). Figure 1. Location of Tubbataha Reefs Natural Park, Sulu Sea. Source: More recent studies have included surveys of the population of Arquiza & White (1999). Brown Booby Sula leucogaster (NRMC 1983, Cruz & White 1989, Arquiza & White 1999) and full surveys of the breeding N bird population in 1991, 1993 and 1995 (Heegaard & Jensen 1992, JESSIE BEAZLEY REEF Magsalay & Toledo 1993, Manamtam 1996). Between 1997 and 0 2.5 5.0 2004, WWF-Philippines made several inventories of the seabird 9.00° N km populations (Sabater 2002, Sabater in litt. 2004). From 2004 until the present day the Tubbataha Reefs Natural Park management Bird Islet office has carried out regular monitoring and made quarterly NORTH ATOLL inventories of the seabirds. Comprehensive surveys, assisted by Plaza independent expert ornithologists, have mainly taken place in May each year (Jensen 2004a, 2005, 2006, 2009, 2010, 2011, 2012, 2013) and are ongoing; this study covers the period up to the end of 2013. Ranger Station E#ective conservation management involving the restriction of Amos Rock access and use of resources from the park started only in 1997. Prior Black Rock Lagoon to that, between the early 1960s and early 1990s, local "shermen Sand SOUTH ATOLL Reef !at/ slope from the Cagayancillo islands, Palawan, stayed for up to a month Reef edge and on the islets to "sh and collect sea-turtles, seabirds, and their eggs, South Islet steep slope Lighthouse mainly between April and July. By the early 1980s, increasing use 120.00° E of motorboats had brought larger numbers of "shermen from other Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 73

overall seabird population is determined by a combination of direct counts of adults, immature and juvenile birds, and square counts of ground-nesting species including nests, eggs, pulli and juveniles. In addition, in-#ight counts, mainly of boobies and frigatebirds, are made between 16h30 and 18h30 (dusk), when most birds congregate and start roosting. Equipment used includes binoculars, spotting- scopes, GPS and digital camera. Distance population monitoring is normally carried out in the morning on a monthly basis from a boat cruising 50–70 m parallel to the shoreline, at both Bird and South Islets, and includes two or three independent estimated counts of all visible seabirds. "e averaged results are used to determine the population variation TERI AQUINO trends throughout the year. A total of 91 distance population counts Plate 1. Aerial photograph of Bird Islet (formerly named North Islet), 25 April 2012. were carried out between April 2004 and May 2013. Of the 66 inventories made on behalf of various organisations between 1981 and November 2013, 13 were between January and March, 31 from April to June, 9 from July to September and 13 from October to December. Most survey e%ort (69%) was put in between 2005 and 2013 and in this period the inventories were made between 13 April and 10 June, mostly from 5 to 10 May. All datasets from 1981 to 2013 were used in the analysis of seabird population trends, and the dataset from June 1981 (Kennedy 1982), taken in late a&ernoon when most of the populations were present, was used as the baseline to determine population trends. "e aggregate counts of populations present on the islets during the day and the birds returning in the late a&ernoon were used to determine the total breeding population of Red-footed Booby Sula TERI AQUINO Plate 2. Aerial photograph of South Islet, 5 September 2005. sula and Brown Booby. Data from the evening in-#ight counts of returning Red-footed and Brown Booby were averaged for the period 548 m measured along the vegetation line and average high-tide 2004 to 2013; for Red-footed Booby, 59.3% of the adult population mark, with a land area of 10,936 m! in 2013 (Jensen 2013). "e was away during the day, and 37.3% for Brown Booby. Appropriate dominant natural vegetation is beach-forest, although about 65% adjustments were made to daytime counts made prior to 2004 of the islet is an open barren area with an in#ux of grasses. "is (Magsalay 1993, Manamtam 1996, Sabater 2002, in litt. 2004) to area, known as the Plaza, is the historical breeding site of ground- facilitate the evaluation of changes to the two species’s populations. nesting seabirds. Analysis of the in-#ight averages using ANOVA (two-factor without "e circumference of the tiny South Islet, area 2,860 m!, in the replication) revealed that the di%erence between years was not South Atoll (8.749°N 119.820°E) is 230 m (Jensen 2013). It was statistically signi$cant (p = 0.024281) within species and age groups. originally part of a large sandbar but a lighthouse, protected by a "us, extrapolation of in-#ight percentages from 2004 to 2013 to the concrete seawall, was constructed in 1978 (Plate 2). Construction of daytime data of earlier years when no in-#ight counts were made was the seawall led to the growth of beach-forest vegetation, including done without compromising the integrity of the datasets. about 100 trees, several of them now up to about 9 m tall. "e results of the seabird inventories collected during the main Jessie Beazley Reef (9.052°N 119.817°E) is submerged at high breeding season from April to June were compared with the datasets tide. At average tides, the exposed area—coral pebbles without from other months to estimate the total annual seabird populations. vegetation—is about 350 m!. Birds have also been recorded on Amos In addition to the counts of seabirds, changes in their habitat use Rock, North Atoll (8.850°N 119.900°E) and Black Rock, South were monitored, with habitat changes being analysed from data Atoll (8.804°N 119.845°E); both are large coralline boulder and collected on the number and status of bushes and trees. From 2004 sand deposits, exposed at low tide. A large bare sandbar at North land areas have been calculated at high tide each year using GPS Atoll, where the park ranger station is located (8.851°N 119.917°E), measurements and changes recorded. also hosts congregations of birds. RESULTS METHODS A total of 106 species has been recorded from the Tubbataha Reefs The Tubbataha Reefs Natural Park management authority Natural Park, of which 11 species breed or are known to have bred, has established a monitoring protocol for seabirds. In 2004, 35 species are Philippine residents or species with both resident and comprehensive training of park rangers and staff from the migratory status, and 60 species are migratory. A complete annotated Tubbataha Management Office was undertaken, focused on list of the birds recorded in the park is given in Appendix 1. identification, monitoring and survey techniques of breeding Accounts of the breeding species, and other species of particular seabirds, based on Bibby et al. (2000). Since then, quarterly direct interest, are given below; land area and habitat changes observed counts of the breeding seabird populations, supplemented by regular during the survey period and the consequences for the avian species distance population monitoring, have become a routine part of of the park are reviewed in the discussion section. the park rangers’ activities. Annual supervision and identi$cation of other bird species is carried out by an independent visiting Selected species accounts ornithologist. "e supervisory function, mainly carried out in early Species marked † are new records for the Philippines and species May, includes a review of the rangers’ monitoring data and an in- marked * are not listed for Palawan province by Dickinson et al. depth inventory focused on the breeding seabird populations. "e (1991) or Kennedy et al. (2000). 74 ARNE E. JENSEN & ANGELIQUE SONGCO Forktail 32 (2016)

Breeding species June 1911, whilst in June 1981 Kennedy (1982) estimated 150 adults !e following 11 species are known to breed or to have bred in the were present. Anthropogenic pressures, including egg and #edgling Tubbataha Reefs Natural Park. collection, caused a terminal population decline (Arquiza & White 1999, Songco 2003). In April 1989 a minimum of 30 adults were * Barred Rail Hypotaenidia torquata recorded (Arquiza & White 1999), whereas on 26 October 1991 First records 5 and 6 May 2003, two adults on both Bird Islet and only 5 adults and 1 immature were present (Heegaard & Jensen South Islet. It is believed to breed regularly on Bird Islet, a pair with 1992) and as late as April 1993 two #edglings were con"scated a nest containing "ve eggs was found there on 30 July 2005; also from a "shing boat (Palaganas & Perez 1993). !e last park record seen there in 2013. (Plate 3) was of one adult on 23 June 1995 (A. Manamtam pers. comm. 1996). !e species is now extirpated from the Philippines; Green-backed Heron Butorides striata the last known record was an immature at sea o$ Camiguin Island, First record 6 May 2004, bred irregularly on Bird Islet and South Cagayan, Luzon, September 2002 (I. Sarenas in litt. 2004). Islet in 2004, 2006, 2007, 2012 and 2013. Evidence of breeding was found on South Islet, 7 May 2007, when a pair was recorded Red-footed Booby Sula sula at a nest (Jensen 2007). !e "rst record for the park, involving eight non-breeding adults, was from South Islet on 15 June 1981 (Kennedy 1982) and this Pacific Reef Egret Egretta sacra was followed by the "rst record from Bird Islet on 25 October First record 24 October 1991, 40 birds (Heegaard & Jensen 1992). 1991 (Heegaard & Jensen 1992). !ere were no further records on Typically 7 pairs breed annually, on both Bird and South Islets; nests either islet until 2000 when two adults were recorded on Bird Islet, hold up to "ve eggs. Of 108 observations, 92 were dark morph birds. followed by 44 in 2001 and 43 in 2002, when three pairs nested for Outside the breeding season inter-island movements may occur (e.g. the "rst time. A breeding colony was established on Bird Islet in 40 birds present in October 1991, 39 in October 2006). April 2004, when there was a huge in#ux of 2,435 adults, and 931 nests were counted. !e following year 4,083 adults and 913 nests Masked Booby Sula dactylatra were counted; numbers then remained in the range 2,500–2,900 Tubbataha Reefs formerly held the only known Philippine breeding until October 2009 when they peaked at 7,047. !e birds nested population of this species (Dickinson et al. 1991, Kennedy et al. in all the available suitable trees and vegetation, sometimes near 2000). Worcester (1911) discovered a large colony on Bird Islet on 29 ground-level but, since the start of colonisation, all mature trees used by the species have died due to loss of foliage—used for nest- Plate 3. The last Masked Booby Sula dactylatra at Bird Islet, May 1995. building—and the e$ect of the birds’ faeces. Colonisation of South Islet did not start until October 2009 (Heegaard & Jensen 1992, Manamtam 1996, Sabater 2002, Jensen 2004a, 2005, 2007, 2009); in May 2010, 90 adults with six nests were counted, whilst in May 2013, 593 adults with 279 nests were counted (Jensen 2013) Data collected by park rangers between 2004 and 2013 con"rmed that the species breeds throughout the year (Table 1, Figure 2), although more nests are found between October and December than earlier in the year, e.g. 931 nests in November 2004 and 1,125 nests in October 2009. !e largest numbers of pulli recorded were 472 in October 2008 and 482 in August 2011. In November 2013, 2,975 adults were counted on Bird Islet, with 494 nests. Data from other colonies indicate that the incubation period is about 45 days and time to #edging 100–140 days (Carboneras et al. 2016); birds generally breed once annually, although seasons may be missed, particularly during El Niño years. !e total annual breeding population is estimated to lie between

J. M. L. TAN 7,000 and 7,500 adults.

Table 1. Red-footed Booby 1981–2013. Maximum counts of adults and nests per year. 1981 1991 1992 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 8 1 0 0 0 0 0 0 2 44 43 20 2,435 4,083 2,625 2,902 2,513 7,047 2,331 3,738 4,487 3,507 Nests 0 0 0 0 0 0 0 0 0 0 3 2 931 913 645 619 710 1,125 459 580 739 848

Figure 2. Red-footed Booby population changes and nesting records 2000–2013. Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 75

Other Philippine breeding sites: the species is known to breed is estimated to be 2,200–2,500 adult birds (Figure 3). !e species at three other sites: Cawili Island, Cagayancillo, Palawan (9.482°N breeds throughout the year, with the highest counts in November 121.036°E), 448 adults (19 nests), 6 May 2007; Bancoran Island, 2011: 588 nests, 167 eggs and 339 pulli, and May 2013: 618 nests, Mapun (formerly Cagayan de Tawi-Tawi), Tawi-Tawi (7.958°N 532 eggs and 28 pulli. 118.666°E), 4,576 adults (314 nests), 16 May 2007; and Bancauan Other Philippine breeding sites: apart from Tubbataha Reefs, Reef, Mapun, Tawi-Tawi (7.763°N 118.525°E), 8,206 adults (2,085 the Philippine breeding population is now restricted to Maender nests), 18 May 2007 (Jensen 2007). Reef, Palawan (8.107°N 118.418°E), 16 adults with "ve nests on 19 May 2007, and Bancauan Reef, Mapun, Tawi-Tawi, six adults Brown Booby Sula leucogaster with two nests on 16 May 2007. Information from the Philippine !e "rst record was from Bird Islet on 29 June 1911, when Worcester Navy indicates that it may still breed on Lawak Island, Kalayaan (1911) recorded an ‘enormous’ population there and noted that Islands, Palawan, but only in small numbers (A. Bundgar pers. the species ‘covered’ South Islet. He also found ‘numerous’ nesting comm. 2005, A. Arca pers. comm. 2006). It is extirpated from pairs on Black Rock—the sandbars around this rock have since Bancoran Reef (Jensen 2007) where it had bred in large numbers disappeared and the area is submerged at high tide (Kennedy 1982, (Worcester 1911) and no is longer found at Didicas Rock, Cagayan, Heegaard & Jensen 1992). !e only subsequent breeding record on Luzon (Allen et al. 2006). South Islet (16 adults) was in June 1981 (Kennedy 1982). From a count of 3,768 adults in June 1981 (Kennedy 1982), the population Greater Crested Tern Thalasseus bergii declined to an estimated 1,000 in April 1989 (White & Calumpong First recorded in June 1911 by Worcester (1911), who reported 1992), followed by a low of 600 in October 1991 (Heegaard & large groups with eggs on Bird Islet. He did not visit South Islet Jensen 1992), then rising to 2,060 in March 1995 (Manamtam but instead found the species breeding in large numbers on nearby 1996) and a high count of 2,402 in 1997 before a new low of 527 Black Rock. In June 1981, when Kennedy counted 1,132 eggs in March 1999 (Sabater 2002). It again stood at only 577 in 2002 (corresponding to 2,264 adults), the species bred only on South Islet, and, although in May 2005 numbers rose to 1,877 (Jensen 2005), but abandoned the islet as a breeding site during the 1980s when they again fell sharply to around 1,000 between 2006 and 2008. the main location, a large barren sandbar, gradually submerged. !e population gradually increased to a count of 2,155 in 2013, still Breeding on South Islet was recorded again in 1995 and between 43% lower than in 1981 (Table 2) and today the adult population 2000 and 2003, with 560 adults counted in 2002; since then

Table 2. Brown Booby 1981–2013. Maximum counts of adults and of nests per year. 1981 1989 1991 1992 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 3,768 1,000 600 2,000 893 2,060 2,402 1,716 527 1,045 850 577 623 847 1,877 1,110 1,016 1,059 1,273 1,442 1,846 1,888 2,155 Nests Present Present 299 Present Present 763 367 225 192 215 69 163 139 117 45 250 89 497 453 513 575 507 618

Figure 3. Brown Booby population and highest numbers of nests 1981–2013

Table 3. Greater Crested Tern 1981–2013. Maximum counts of adults and eggs per year. 1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 2,264 100 18 335 15 0 0 2,300 414 4,160 2,064 2,808 7,858 6,894 4,700 6,000 4,433 4,790 6,160 8,653 10,500 Eggs 1,132 0 0 135 0 0 0 97 0 411 109 0 3,929 3,590 521 0 515 2,341 498 1,456 3,939

Figure 4. Greater Crested Tern population and highest numbers of eggs 1981–2013. 76 ARNE E. JENSEN & ANGELIQUE SONGCO Forktail 32 (2016)

up to 640 adults have been recorded in May counts but, despite February to July, whilst a smaller population (absent in 2004, 2006 some displaying, there has been no evidence of breeding. In 1981, and 2012), averaging 2,400 individuals, breeds from September Kennedy (1982) found no breeding birds on Bird Islet, although the to November. !e species is usually absent from the park from species was present there in 1982, 1989, 1991 and 1993 (NRMC December to the end of February, except in February 2011 when 1983, Heegaard & Jensen 1992, Magsalay & Toledo 1993), but 1,585 pulli were recorded, indicating that breeding started as early breeding was not recorded until 1995 (Manamtam 1996) or again as December the previous year. When adults return to Tubbataha until August 2000, when 2,300 adults were present with juveniles Reefs, they continue to be pelagic by day, settling on land at night (Sabater 2002). !e population has since "uctuated, although it for courtship and territorial claims; this continues for 6–7 weeks increased to 9,154 adults with 3,939 eggs in May 2013. !e highest before egg-laying starts. Since the counts are made during the hours number of pulli (2,540) was recorded in July 2006. Overall, the of daylight, the numbers of birds from the beginning of the breeding population decreased from 2,264 in 1981 (Kennedy 1982) to only season may be an under-estimate. The total annual breeding 335 in 1995, but recovered to reach 10,500 adults in August 2013 population in peak years is estimated to be 15,000–16,000 adults. (Table 3, Figure 4). !e highest spring breeding count was 10,866 adults with 5,515 eggs Greater Crested Terns breed mainly from May to August and in May 2010 (Table 4, Figure 5), and the highest autumn breeding in some years from October to November (2004–2006, 2009). It count was 4,331 adults in October 2009. In July 2006, 3,100 pulli is generally absent from the park between December and March. were counted, with 7,920 adults. From October to December the breeding population is smaller, with Other Philippine breeding sites: the only other breeding site a peak count of 2,000 individuals in November 2004. Based on is Lawak Island, Kalaayan, Palawan (McManus 1994, P. Aliño in the peak counts of the two breeding populations, the total annual litt. 2009), where breeding numbers are thought to be greater than population is estimated to be between 12,000–12,500 adults. at Tubbataha Reefs; in 2005 the seasonal egg harvest was 16 large Other Philippine breeding sites: breeding was reported from baskets (A. Bungar pers. comm. 2005). Maender Reef, Palawan, where numerous groups were noted in June 1911 (Worcester 1911) but not in June 2002 (Sabater 2002); Brown Noddy Anous stolidus however, in May 2007, 210 adults with four nests were seen (Jensen !e #rst record was in June 1911 when Worcester (1911) reported 2007). !e species may breed in small numbers at Sinamahan Cay, numerous birds nesting on Bird Islet. In June 1981, 1,100 adults Balabac (Matillano et al. 2006), but is now extirpated from Bancuan were counted there by Kennedy (1982), who also found 518 nests on Reef, Mapun, Tawi-Tawi, where more than 100 pairs bred in 1985 South Islet. However, in October 1991 Heegaard & Jensen (1992) (Caretaker M. Bantala pers. comm. 2004). found only 25 non-breeding birds on Bird Islet and 65 non-breeders on South Islet; in 1993 Magsalay & Toledo (1993) found 200 adults Sooty Tern Onychoprion fuscatus on Bird Islet and 15 on South Islet, whereas in 1996 Manamtam !e #rst record by Kennedy (1982) was of 35 non-breeding adults on (1996) found about 600 adults on Bird Islet and 43 on South Islet, Bird Islet on 13 June 1981; he subsequently reported 5,000 breeding several of them with nests. On Bird Islet, only 37 bred in 2001, 375 adults on South Islet (Kennedy 1982). It disappeared from South in 2002 but none in 2003. However, from 2004 the species bred Islet as a breeding species during the 1980s, apparently due to the annually in increasing numbers, from 216 birds in 2004 to 1,742 in loss of suitable breeding habitat, and there is only one subsequent 2011, before declining to 1,163 in 2013. A high count of 573 nests breeding record from here, 23 adults on 26 May 2002 (Sabater holding 405 eggs was made in May 2013. !e species was absent 2002). On Bird Islet it was reported to be present in 1982 (NRMC from South Islet in 1998, 1999 and 2001 but, with 40 recorded 1989) and in October 1991 more than 830 pulli, equivalent to about in 2000 and 450 in 2002 (Sabater 2002), 115 in 2003 and 868 in 1,660 adults, were noted there (Heegaard & Jensen 1991), whilst in 2006; in 2013, adults numbered 525. March 1995, 455 juveniles were counted among adults (Manamtam !e population declined from the 2,136 individuals recorded 1996). In the 1990s and early 2000s the population on Bird Islet in June 1981 and, a$er 30 years of "uctuation, only returned to this was subject to large "uctuations and the species was largely absent order of magnitude in May 2011. It was absent in 1998 and 1999 but and did not breed in 1998 and 2003, but it has bred continuously present in "uctuating numbers every year since 2000. !e species is there since 2004, albeit in small numbers in some years. present from late April to early November, breeding mainly from There are two subpopulations of Sooty Terns breeding on May to August, although more than 300 juveniles were recorded Bird Islet: the larger population normally breeds from the end of in late October 2009 (Table 5, Figure 6).

Table 4. Sooty Tern 1981–2013. Maximum spring counts of adults and eggs/pulli per year. 1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 5,035 1,660 11 910 3,570 28 6,500 3,450 6,224 2,123 2 1,200 3,500 7,920 1,500 3,800 2,700 10,866 6,335 6,359 3,771 Eggs/pulli 2,500 830 0 455 1,625 0 3,393 384 516 366 0 9 1,750 3,960 521 2 849 5,515 2,665 1,534 1,404

Figure 5. Sooty Tern population and highest numbers of eggs/pulli 1981–2013. Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 77

Other Philippine breeding sites: in the Sulu Sea the species is of 7,128 adults. "e Bird Islet population then $uctuated between restricted to Maender Reef, Palawan, where 90 adults (six pairs with 3,250 and 4,552 in the period 1997–2000 before about 7,000 were nests) were recorded on 19 May 2007 (Jensen 2007). Photographic recorded in 2001, although it then collapsed to about 800 in 2004. documentation and interviews with navy personnel indicate that In 2005 most of the breeding population were still on Bird Islet more than 300 individuals breed on Lawak Island, Kalayaan Islands, (6,400 adults) but therea%er the Bird Islet breeding population from February (A. Arca pers. comm. 2006, P. Aliño in litt. 2009). declined, probably due to loss of habitat—only about 2,500 adults It may breed on Manlanat (Lantao) Island, Jomalig, !uezon (J. C. were present there in May 2013. As numbers declined on Bird Islet, T. Gonzalez in litt. 2002). those on South Islet increased correspondingly—215 in October 2005, 3,300 in 2006 and 8,250 in 2013, when a record number of Black Noddy Anous minutus 10,656 adults were counted in May on both islets (Table 6, Figure 7). "e subspecies worcesteri, #rst found on 24 September 1910 on "e Black Noddy breeds mainly from late April to August and, Cawili Island, Cagayancillo, Palawan (Worcester 1911), now breeds in 1991, 1997, 2008 and 2009, also bred from September to October; on Tubbataha Reefs. "e #rst record was of 147 adults on South it is normally absent from Tubbahata Reefs between November Islet in June 1981 (Kennedy 1982); birds were also present there but and March. "e October breeding population is the smaller of the did not breed in 1993 and 1999. However, it bred on South Islet in two, with peak counts of 3,500 individuals in October 1997 and small numbers between 2000 and 2002 and started breeding there 2,700 individuals in October 2009. Based on peak counts of the again from October 2005, when 215 adults were counted; numbers two breeding populations, the total annual population is estimated then rose from 3,300 in 2006 to 8,250 in 2013. "e species was #rst to be between 12,000 and 13,000 adults. documented on Bird Islet in May 1991 (Palaganas & Perez 1993), Other Philippine breeding sites: the only other known breeding when large numbers were breeding in the lettuce trees and where, in site is Cawili Island, Cagayancillo (Kennedy et al. 2000). According October 1991, Heegaard & Jensen (1992) counted 1,503 nests with to a resident who had lived on the island since 1959, the species almost fully-$edged juveniles, equating to about 3,000 breeding abruptly disappeared in 1987 (W. Dosong pers.comm. 2007). adults. In May 1993 Magsalay & Toledo (1993) recorded a total of 2,230 adults, the majority of which were breeding on Bird Islet. Eurasian Tree Sparrow Passer montanus In June 1995 Manamtam (1996) found 3,564 nests on Bird Islet, First recorded from Bird Islet on 25 October 1991 (Heegaard & containing 713 pulli and 1,070 eggs—equivalent to a population Jensen 1992); six to eight birds now breed there annually. Recorded

Table 5. Brown Noddy 1981–2013. Maximum counts of adults and nests per year. 1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 2,136 90 215 643 175 0 0 500 37 775 115 336 834 1,228 750 860 1,570 1,775 2,042 1,492 1,688 Nests 518 0 0 20 54 0 0 83 11 134 45 115 75 416 56 334 384 655 924 709 771

Figure 6. Brown Noddy population and highest numbers of nests 1981–2013.

Table 6. Black Noddy 1981–2013. Maximum counts of adults and nests per year. 1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Adults 147 3,006 2,230 7,128 3,500 3,250 3,850 4,552 6,998 4,860 1,500 805 6,619 7,620 6,250 6,890 7,305 7,644 8,351 9,436 10,656 Nests Present 1,503 Present 3,564 1,023 901 1,564 863 1,876 1,615 0 208 3,374 3,700 2,718 1,824 2,680 3,525 3,827 4,282 5,156

Figure 7. Black Noddy population and highest numbers of nests 1981–2013. 78 ARNE E. JENSEN & ANGELIQUE SONGCO Forktail 32 (2016)

on South Islet since 2010, with up to eight individuals present. !e Simon and Candaba, Pampanga, Luzon; and the Hundred Islands species also occurs irregularly at the Ranger Station. National Park, Pangasinan, Luzon (WBCP 2003, 2004, 2007, 2008, 2009, 2012). Other species of particular interest Chinese Egret Egretta eulophotes (VU) * Northern Shoveler Spatula clypeata First recorded from Bird Islet on 23 March 1995 (Manamtam 1996). One record, from the Ranger Station on 26 October 2006 (WBCP !ere were eight subsequent records of up to three birds, between 2006). An uncommon migrant to the Philippines in suitable April 2006 and May 2012. Sixteen individuals were recorded on habitats (Kennedy et al. 2000). Bird Islet, two at the Ranger Station, and one on South Islet. A rare migrant in the Philippines, recorded in declining numbers, with White-tailed Tropicbird Phaethon lepturus most records from the Visayas, central Philippines (Kennedy et al. One record, an adult between North Atoll and Jessie Beazley Reef, 2000, DENR-PAWB 2012). 1 May 2006. An apricot tinge on the elongated tail feathers, lower belly and undertail-coverts, suggested subspecies dorothea, although Great Frigatebird Fregata minor ful!us could not be ruled out. !e seven Philippine records include !e species is listed for Bird and South Islets of Tubbataha Reefs one from Palawan, on 19 June 1995 at Sultana Shoal, Cagayancillo by Kennedy et al. (2000) but without further details. !ere are no (Manamtam 1996, WBCP 2008, 2012). !e species, widespread records of the species in Kennedy (1982). A 1995 record is undated in the Paci"c, is considered to be accidental in the Philippines (Manamtam 1996). (Kennedy et al. 2000). Bird Islet: the first dated record was of six adults and one immature, 5 May 2001 (Sabater 2002). Since then the species has * Buff-banded Rail Hypotaenidia philippensis been recorded throughout the year, with peak counts of 28 adults One record from Bird Islet, 14 May 2010, and one other Palawan and two immature birds on 10 June 2002 and 21 adults and 7 record from Coron Island, 16 February 2009 (WBCP 2009). !e immatures on 8 May 2005. Numbers had fallen to just "ve adults in species is a locally common resident in other parts of the Philippines 2013, apparently due to the decline and subsequent disappearance (Kennedy et al. 2000). of tall trees used for roosting. South Islet: not recorded before 2011. On 8 May 2013, 13 adults † Swinhoe's Storm Petrel Hydrobates monorhis (NT) and three immature birds were observed. !e appearance of the !e "rst Philippine record of this Near !reatened species, on 11 species here may be associated with kleptoparasitism of the newly May 2013, involved a bird at sea (9.136°N 119.614°E), 20 km west- established colony of Red-footed Booby and the presence of tall north-west of Jessie Beazley Reef (Jensen et al. 2015). !e species trees suitable for night roosts. breeds as close as on small islets o# Taiwan and over-winters in the !e species’s resident status in the Philippines is based on a Indian Ocean (Birdlife International 2015). It is likely that it is historical claimed breeding record from Cawili Island, Cagayancillo, regular although perhaps rare or uncommon in Philippine waters. Palawan (Worcester 1911). Worcester did not "nd nests or eggs but based his conclusion on the presence of immature birds and * Wedge-tailed Shearwater Ardena pacifica some males with pu#ed-out scarlet pouches. He wrote, ‘the species First record, one at sea o# South Islet, 24 October 1991 (Heegaard apparently had "nished nesting but immature birds were present & Jensen 1992). !ere are four subsequent records from the park: in large numbers’, and recommended a visit to Cawili Island ‘in an undated 1995 record (Manamtam 1996); one near Jessie Beazley the season where possibly the frigate birds would be found mating’. Reef, 11 May 2005; one injured bird on Bird Islet, 27–29 October According to Wilfredo Dosong (pers. comm. 2007), a resident of 2007; and one over the open sea o# North Atoll, 6 May 2008. Other Cawili Island since 1959, the species had not bred on the island in records from Palawan province include an unpublished record his time, although both immature and adult birds were present of one 25 nautical miles o# Palawan, 26 June 1980 (Gast 1999), throughout the year. At the country’s largest known frigatebird roost, one o# Cagayancillo Island, 6 May 2007, and one near Calusa on Bancauan Island, Mapun, Tawi-Tawi, the senior caretaker claimed Island, Cagayancillo, 8 May 2008 (WBCP 2007, 2008). Although that in around 1985 the species bred from December onwards. considered to be an accidental, rare pelagic species (Kennedy et al. However, despite a search for nests and other evidence of breeding on 2000), more than 100 records since 2004, e.g. from Cagayan and 17–19 October 2004 and 16 May 2007, no nesting birds or nests were Surigao provinces, suggest that, although uncommon, it is a regular found (Jensen 2004b, 2007). In the absence of con"rmatory data, migrant to the Philippines (Allen et al. 2006, WBCP 2010, P. it appears more likely that the species is migratory, with the main Bourdin in litt. 2013). distribution in the Sulu Sea. Frigatebirds are biennial breeders— young birds are dependent on adults for more than a year—hence Japanese Night Heron Gorsachius goisagi (EN) the year-round presence of adults at Tubbataha Reefs and elsewhere One record of this Endangered species from South Islet, 10 in the Sulu Sea should not be taken as indicative of local breeding. May 2005, an adult found dead (Jensen 2005). !e following !e majority of records on both Cawili and Bancuan Islands are of measurements were taken: bill: 44 mm, tarsus: 66 mm, wing: immatures (Jensen 2004b, 2007), suggesting that these birds are 267 mm. Rare migrant recorded from north, central and south present in the Philippines until they reach maturity. Philippines, including Palawan (Kennedy et al. 2000). * Christmas Frigatebird Fregata andrewsi (CR) * Black -crowned Night Heron Nycticorax nycticorax Only recently con"rmed for the Philippines, the species has been One record, an immature bird at the Ranger Station, 15 May 2010. seen only in the Sulu Sea (Jensen & Tan 2010), except for one !ere is an unpublished record from Santa Lourdes Beach, Puerto record, 22 January 2013, La Mesa Dam, $uezon City, Metro Manila Princesa, Palawan, on 17 May 1980 (Gast 1999), and an immature (Jensen et al. 2015). In the Sulu Sea it has been documented from bird was on Bancoran Island, Mapun, Tawi-Tawi province, on "ve Philippine islets and eight adjacent islands and islets o# Sabah, 19 May 2007 (A. Manamtam in litt. 2007). Although listed as Malaysia (Jensen 2007). Bancauan Island, Mapun, Tawi-Tawi, migratory (Dickinson et al. 1991, Kennedy et al. 2000), since 2003 where up to 70 birds, both juveniles and adults, have been observed, breeding colonies have been documented, e.g. Baras Bird Sanctuary, is an important roost site (Jensen 2004b, 2007, Jensen & Tan 2010). Sultan Kudarat, Mindanao; Paranaque City, Metro Manila; San Frigatebirds normally congregate in the greatest numbers just before Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 79

dusk; juvenile Christmas Frigatebirds may consequently have been counts made: two in January, one in March, two in April, 14 in May, overlooked in mixed frigatebird !ocks. one in August, three in October and two in November. "e counts First record from Bird Islet, 5 May 2003, an adult female and a resulted in a total of 870 birds, of which 691 were recorded on Bird juvenile (Norwin Abes in litt. 2004). "ere were 29 records between Islet and 179 on South Islet. Most birds were seen during southward May 2003 and May 2013: 16 adults (15 females and one male), migration, with a peak count of 174 individuals in October 1991. ten immatures (3 males and 7 female) and only three juveniles, "e highest count during northward migration was 95 in March estimated to be one to two years old, have been identi#ed (Jensen and a winter high count of 47 occurred in January 2006. & Tan 2010, Jensen 2011, 2012). "e average number of birds counted in April and May, arranged in 5-year intervals between 1999 and 2013, was 24 individuals Eurasian Curlew Numenius arquata (NT) annually for the decade 1999 to 2008. However, the average for One record from Bird Islet, 26 October 1991, comprised four birds 2009 to 2013 was only #ve birds annually. "e number of birds (Heegaard & Jensen 1992). Locally uncommon migrant, recorded during the southward migration period dropped from 174 in from north, central and south Philippines, including Palawan October 1991 to 94 in October 2006. Although the data are (Kennedy et al. 2000). limited, they suggest either a change in migration phenology or that the population over-wintering in and transmigrating through * Black-tailed Godwit Limosa limosa (NT) Tubbataha Reefs is undergoing a decline First record of 11 birds on 26 October 1991 (Heegaard & Jensen 1992), then one on 28 October 2006 and one on 7 May 2008 (all * Pomarine Skua Stercorarius pomarinus from Bird Islet). A rather rare and local migrant in the north and One record of a light phase adult passing South Atoll on 10 May central Philippines, there are internationally important roost sites 2005. A bird passing North Atoll on 8 May 2009 may have been of this Near "reatened species on Negros Occidental and Cebu this species. Additional records from the Sulu Sea include one at (Kennedy et al. 2000, DENR-PAWB 2012). Manuc Manucan Reef (7.717°N 118.450°E), Mapun, Tawi-Tawi, 21 October 2004 (WBCP 2004); two between Cagayancillo and * Bar-tailed Godwit Limosa lapponica Cawili Islands, Cagayancillo, Palawan, 6 May 2007 (WBCP 2007); One record of three birds from Bird Islet, 26 October 1991, and one and up to 50 o% Patikul (6.089°N 121.105°E), Jolo Island, Sulu, 19 there, 7 May 2008. According to Kennedy et al. (2000), the species December 2012 (WBCP 2012). Although listed as a rare migrant is an uncommon migrant in the Philippines. (Kennedy et al. 2000), records since 2004 con#rm that the species occurs annually in the Philippines (WBCP 2004, 2005, 2008, * Red Knot Calidris canutus 2010, 2011, 2012). One record from Bird Islet, 26 October 1991. According to Kennedy et al. (2000), the species is an uncommon migrant in the Philippines. * White-throated Kingfisher Halcyon gularis One record from South Islet of a single taken by a Peregrine Falcon * Sanderling Calidris alba Falco peregrinus, 30 April 2006. "e species is a fairly common "ree records from Bird Islet, on 29 April 2006, 7 May 2007 and 8 resident in the Philippines (Kennedy et al. 2000). May 2011, and one from South Islet on 30 April 2006. Four other Palawan records: three birds, Pandan Island, Honda Bay, Puerto * Oriental Skylark Alauda gulgula Princesa and one, Sabang Beach, Puerto Princesa, in April 2008 One record of a bird passing northwards at the Ranger Station, (WBCP 2008); one bird, Manamoc Island, Cuyo Archipelago, 23 8 May 2005. An uncommon resident in the Philippines, but no April 2010 (WBCP 2010); and one, Arrece$ Island, Honda Bay, information about inter-island movement (Kennedy et al. 2000). Puerto Princesa, 12 November 2011 (WBCP 2011). "e species is an uncommon migrant to the Philippines (Kennedy et al. 2000). * Clamorous Reed Warbler Acrocephalus stentoreus One individual was caught in a mist-net on South Islet, 10 May Grey-tailed Tattler Tringa brevipes (NT) 2005, and released the same day. It is an uncommon resident in Eighteen counts, one in October 1991 and 17 between 1999 and the Philippines, but there is no information about inter-island 2013, recorded 502 individuals— 412 from Bird Islet and 90 from movement (Kennedy et al. 2000). South Islet. Fourteen of the counts were made in April–May, one in March, one in September and two in October. Most sightings Purple-backed Starling Agropsar sturninus occurred during southwards migration, with a peak count of 237 One record from Bird Islet, 26 October 1991, two birds observed birds in October 1991. Peak counts during northwards migration (Heegaard & Jensen 1992); the second of only three Philippine were 43 birds in both March 1991 and May 2004. records (Jensen et al. 2015). The average numbers of birds counted, arranged in 5-year intervals between 1999 and 2013, shows a declining trend: 21 † Rosy Starling Pastor roseus individuals annually in 1999–2003, 17 annually in 2004–2008, First Philippines record from South Islet, 10 May 2009, one adult in and just two annually in 2009–2013. "e number of birds during non-breeding plumage. Two subsequent records (Jensen et al. 2015). the southward migration dropped from 237 individuals in October 1991 to 65 in September 2000 and just eight in October 2006. Yellow Wagtail Motacilla flava Recent evidence suggests that the global population of the A male of subspecies macronyx on Bird Islet, 7 May 2005, was the species declined between 1987 and 2011 and it is currently listed as #rst record of this taxon from the Philippines (Jensen 2005). It was Near "reatened, due to an estimated overall decline of 20–29% in identi#ed by its uniform grey crown and ear-coverts, the absence Australia over the last 25 years (van Gils & Wiersma 2014). Numbers of a supercilium, green upper back, bright yellow underparts and migrating through Japan in autumn have declined by 57% between distinctive whitish wing-bars. Subspecies macronyx breeds from 1983 and 2007 (Amano et al. 2010). Transbaikalia, Amurland and Ussuriland, Far East Russia to Mongolia, Manchuria and China and winters in South-East Asia Ruddy Turnstone Arenaria interpres and south-east China (Tyler et al. 2016). "e earliest counts are from October 1991 and March 1995. "e A male tschutschensis Yellow Wagtail recorded on Bird Islet species has been recorded in every year from 1997 to 2013, with 25 on 14 May 2010 was the #rst Philippines record of this taxon, and 80 ARNE E. JENSEN & ANGELIQUE SONGCO Forktail 32 (2016)

another male was there, 9–10 May 2013 (Jensen 2010, 2013). !e per year (Bindo% et al. 2007). Since 1990, the number of tropical bird showed a pale grey head, blackish ear-coverts and a long white cyclones in the west Paci&c has increased, although the number of supercilium. Subspecies tschutschensis breeds from north-east Siberia resulting typhoons making landfall on the Philippines has remained to the most easterly parts of north-eastern Russia and western and constant at about 20 per year. However, the typhoon path, intensity northern parts of Alaska, and winters mainly in South-East Asia and duration have changed—today more typhoons make landfall south to most of the Indonesian islands (Tyler et al. 2016). on the central Philippines and also impact the previously relatively typhoon-free Sulu Sea (Emmanuel 2007). !e rise in sea-level, . together with the increased frequency and intensity of storms DISCUSSION crossing the Sulu Sea, appear to be the main factors that are causing the changes in land area. Changes in sea currents are a contributory Changes to land area factor, causing major movements of sand deposits, which have led Bird Islet (formerly known as North Islet) has undergone major to the emergence of numerous temporary sand cays in the reef "ats changes since June 1911, when it was a ‘low "at sandy island some of the atolls, the disappearance of the major sandbars at Black Rock 400 meters long by 150 wide’ (Worcester 1911); by 1981 it was and around South Islet and, between 2008 and 2010, a substantial described as 268 m long and 70 m wide at high tide (Kennedy 1982). decrease in the area of a major sandbar adjoining Bird Islet (Kennedy !e area of the islet has decreased from an estimated 60,000 m# in 1982, Aquino et al. 2011, Jensen 2013). 1911, to 18,760 m# in 1981, 17,000 m# in 2004 and about 10,930 m# in 2013 (Jensen 2013). A$er a change of only 9% between Habitat changes 1981 and 2004, the following 10 years to 2013 saw a further 35% Both Bird and South Islets have changed progressively from barren reduction—blocks of the sandstone, with surface soil, up to 1 m# in to fully-vegetated habitats, in"uencing the make-up of breeding bird area, are now broken o% the islet by wave action during high tides or species. !e vegetation is now predominantly lettuce tree Pisonia alba stormy weather (Plate 4). !is severe erosion has seriously damaged and octopus bush Argusia argentea with tropical almond Terminalia the south and north-west shorelines and reduced the area available catappa, and a few stands of coconut palm Cocos nucifera. Butter daisy to the ground-nesting boobies (Kennedy 1982, Jensen 2006). Melampodium divaricatum, purslane Portulaca oleracea, purple-top South Islet, in contrast, is relatively stable due to the concrete chloris Chloris in!ata and Setagaria geniculata also occur (Kennedy seawall constructed in 1978, although an adjacent wide barren 1982, Palaganas & Perez 1993, Jensen 2007). sandbar, which hosted dense tern colonies in 1981 (Kennedy In 1911, Bird Islet was barren, except for a few stands of purslane 1982) has disappeared. Other changes in land area include the (Worcester 1911), and remained so for the next 70 years (Kennedy disappearance of an unnamed sandy islet at Black Rock on the 1982). By 1991 dense young beach-forest with more than 100 South Atoll (Worcester 1911, Kennedy 1982). trees had developed on the north, east and south-east shorelines Global sea-levels rose at a mean rate of 1.8 mm per year for the (Heegaard & Jensen 1992); bush and tree numbers increased to past century (Douglas 1997, Church & White 2006); however, about 500—many up to 9 m tall—by 2004. However, since then between 1993 and 2003 rates have been estimated to be 2.8–3.1 mm the massive in"ux of breeding Red-footed Boobies has destroyed this habitat; by 2013 nearly all mature trees were dead and bushy Plate 4. Bird Islet, 9 May 2013. Erosion has caused a decrease in land vegetation was deteriorating due to the activities of this species area of more than 40% since 1981. (Jensen 2013). !e destruction of vegetative cover by Red-footed Boobies caused most of the Black Noddies, which had nested in the lettuce trees since 1991, to move to South Islet (Jensen 2013). On Bird Islet in 1991 there was an 8,000 m# open grassy area known as ‘the Plaza’ (Heegaard & Jensen 1992), which was the historical breeding site of ground-nesting seabirds. By 2002 it had been reduced to only about 1,100 m# by the rapid spread of introduced tamarind Leucaena leucocephala (White et al. 2004). In 2007 tamarind was eradicated by the park sta% and the Plaza (Plate 5) has expanded to 4,840 m# (Jensen 2013). Species which use trees for night roosts, such as frigatebirds, including the Critically Endangered Christmas Frigatebird, have bene&ted from the increased vegetative cover. Conversely, the increased vegetative cover that resulted from the building of the seawall on South Islet when the lighthouse was built in 1978 may have contributed to the decline and subsequent disappearance of the ground-breeding Greater Crested Tern and Sooty Tern from that location. South Islet was largely barren in 1981, apart from a few bushes (Kennedy 1982). In 1991 Heegaard & Jensen (1992) found considerable native beach-forest vegetation with relatively tall trees with thick foliage, together with dense bushy vegetation (Plate 6). In 2013 there were about 130 trees, although since 2011 the condition of nearly half of them has deteriorated due to the presence of breeding Red-footed Boobies (Jensen 2013).

Changes in the breeding seabird population !e park is the only known breeding area of the subspecies worcesteri of the Black Noddy. !is taxon formerly bred on Cawili Island until 1987 and may also occur on Ashmore Reef, north-west Australia (Gochfeld et al. 2016). Within the Philippines it hosts the only

ARNE E. JENSEN major colony of Brown Booby, the second-largest populations of Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 81

From about 13,540 adults of all species in 1981, the breeding population decreased to about 5,450 in 1991, a 60% decline. It increased to more than 11,000 in 1995 before again declining to only about 4,990 in 1998. Between 1999 and 2002 the average breeding population increased to 12,460 individuals but in 2003 the population was just 4,320 individuals, less than a third of Kennedy’s count in 1981. However, since 2004 there has been a gradual population increase to an all-time high of about 32,300 individuals in 2012 and 2013, 138% higher than the "rst count of 1981 (Figure 8). There are significant differences in the population trends of tree-nesting and ground-nesting seabirds. !e population of ground-nesting species in 2013 was 35% higher than in 1981. !is is due to an increase in the Greater Crested Tern population from about 2,260 individuals in 1981 to nearly 10,500 in 2013. Other species had lower populations in 2013 than in 1981: the Brown ARNE E. JENSEN Booby population (2,155) is 43% lower and the Brown Noddy Plate 5. Bird Islet, May 2013. The main breeding ground for Brown Booby Sula leucogaster and Greater Crested Tern Thalasseus bergii at the Plaza. population (1,688) is 21% lower. !e Masked Booby population In the background are dead trees killed by the high breeding density declined rapidly in the 1970s and by 1981 numbered only 150 of Red-footed Booby Sula sula. adults; it was extirpated from Tubbataha Reefs Natural Park, and the Philippines, in 1995. Because of the growth of suitable habitats for the tree-nesting Black Noddy and Red-footed Booby, these two species have undergone a remarkable increase: from only 147 Black Noddies in 1981 to about 10,650 in 2013, and from just six breeding Red- footed Boobies in 2002 to about 4,490 in 2012. It is probable that the Black Noddy population originated from Cawili Island, from where it disappeared abruptly in 1987 (W. Dosong pers. comm. 2007). A large number of "shermen settled on Cawili Island from 1975 to 1977, increasing the killing of seabirds and converting most of the beach-forest on the island to agricultural lands (Arquiza & White 1999), which may explain the species’s disappearance from Cawili Island and the corresponding breeding in large numbers on Tubbataha Reefs (Palaganas & Perez 1993). !ere have been considerable #uctuations between some years in the breeding numbers of Greater Crested Tern, Sooty Tern and Brown Noddy. !ere was an apparent absence of these species

ARNE E. JENSEN in 1998, of Greater Crested and Brown Noddy in 1999, and of Plate 6. South Islet, 8 May 2013. Dense vegetation with breeding Black Sooty Tern again in 2003, whilst in some years there are unusually Noddy Anous minutus. high breeding numbers of Greater Crested Tern (2005–2006 and Red-footed Booby and Sooty Tern, and the largest breeding colonies 2012–2013) and of Sooty Tern (1999, 2001, 2006, 2010 and 2012). of Greater Crested Tern and Brown Noddy. !ese population peaks could indicate irregular population trends Using the count results from June 1981 (Kennedy 1982) as a which may be associated with sea-surface temperature variations, baseline to determine variations and trends over time, it can be as concluded by Devney et al. (2009). !ey found that population concluded that there have been considerable changes in the seabird declines of pelagic seabirds were related to the frequency and populations of the park. !e number of breeding seabird species intensity of El Niño anomalies in the western tropical Paci"c. declined from seven in 1981 to six by 1995 and the ranking of the !ere have been eight moderate to strong El Niño and four La three most abundant species in 1981—Sooty Tern (5,070), Brown Niña events since seabird data collection started at Tubbataha Reefs Booby (3,768) and Greater Crested Tern (2,264)—changed over in 1981 (Null 2014, WMO 2014). !e absence of breeding Greater the period to 2013 to Black Noddy (10,656), Greater Crested Tern Crested Terns and Brown Noddies in 1998 to 1999 and of Sooty (10,500) and Sooty Tern (3,771). Terns in 1998 coincides with the El Niño/La Niña anomalies in

Figure 8. Breeding seabird population trends in Tubbataha Reefs Natural Park 1981–2013. 82 ARNE E. JENSEN & ANGELIQUE SONGCO Forktail 32 (2016)

1997 to 1999, while an El Niño period in 2002 to 2003 coincided Tubbataha Reefs Natural Park provides opportunities for avifaunal with the absence of Sooty Terns in 2003. research that could #ll gaps in our knowledge and further enhance Devney et al. (2009) showed that El Niño generated sea-surface the e"ective conservation and management of seabirds. temperature anomalies and ‘intense El Niño events can severely impact seabird populations, often months in advance of peak temperature anomalies’. Recent phenological analysis of seabird ACKNOWLEDGEMENTS data from Tubbataha Reefs by Carcallas (2013) suggests that the higher the chlorophyll concentration, which occurred in January We dedicate this paper to the Tubbataha Reef Natural Park marine rangers to March, the earlier the Sooty Terns start egg-laying, while the employed by the Philippine Navy, the Philippine Coast Guard, the Tubbataha peak sea-surface temperature was strongly linked to the start of egg- Management O&ce and the Municipality of Cagayancillo, who have been laying for the Greater Crested Tern. However, the overall increase instrumental in collecting the data presented herein, and to Tim Fisher, in the sea-surface temperature did not negatively in!uence the adult whose untimely passing has le' our endangered seabirds with one less zealous seabird population in the park over time. advocate. Special thanks go to Noel Bundal, Segundo Conales and Roy Magbanua for consistent and untiring data collection. We thank the Tubbataha Factors affecting the seabird population Protected Area Management Board and WWF-Philippines for logistical Negative anthropogenic factors a"ecting seabirds included the support for the annual May inventories. We thank Marivel Dygico, Captain seasonal collection of eggs and chicks and frequent disturbance Ronald de Roa and the crew of the WWF research vessel M/Y Navorca for of the breeding colonies by visiting #shermen and scuba divers their participation in the surveys and for safe enjoyable passages to and from up to 1998, when the islets were closed to visitors. Park sta" have Tubbataha. Special thanks to Teri Aquino, Robert Brinks, Melvin Calderon, documented a growing number of avian casualties caused by marine Anton Carag, Cristobal Cayetano, Robert Hutchinson, Godfrey Jakosalem, debris, which may cause many fatalities through entanglement in Arturo Manamtam, Maia Melacio, Nadia Palomar, Lisa-Marie Paguntalan, discarded or lost #shing gear and the ingestion of toxic chemicals Sylvia and Tonji Ramos and Gregg Yan, who provided valuable volunteer from degrading plastics (Pierce et al. 2004, Gregory 2009, Eidt assistance during the #eldwork from 2004 to 2013. Our sincere appreciation 2012, Lavers & Hutton 2014). In Tubbataha Reefs Natural Park goes to Teri Aquino for permission to use her images. $e dra' manuscript was marine !otsam, particularly plastic, is increasingly used as nesting critically reviewed by David James whose expert comments greatly improved material by seabirds. Other factors affecting seabirds include its accuracy. climate-change related variations in sea-surface temperature, changes in severity and movement patterns of typhoons, and a rise in sea-level, causing breeding failure and reducing the area available REFERENCES to birds for breeding. Both Worcester (1911) and Kennedy (1981) encountered egg- Allen, D., Espanola, C., Broad, G., Oliveros, C. & Gonzalez, J. C. T. (2006) New collectors during their brief visits. Many #shing crews survived bird records for the Babuyan islands, Philippines, including two first on #sh, birds and their eggs taken from Tubbataha Reefs, while records for the Philippines. Forktail 22: 57–70. commercial dive-boat crews were observed with drums full of Amano, T., Szekely, T., Koyama, K., Amano, H. & Sutherland, W. J. (2010) A seabird eggs (Kennedy 1982, Arquiza & White 1999). $e frequency framework for monitoring the status of populations: an example from of disturbance and egg collection by visiting divers and #shermen wader populations in the East Asian-Australasian flyway. Biol. Conserv. intensi#ed during periods of good weather from March to May 143: 2238–2247. and in October. Heegaard & Jensen (1992) found 25 #shing vessels Aquino, M. T. R., Alarcon, R. C. & Pagliawan, M. R. C. (2011) Vulnerability and from Cagayancillo, Cebu and Taiwan anchored around Bird Islet resilience assessment of Tubbataha Reefs Natural Park, Cagayancillo, in October 1991, with nearly 80 people in and around the breeding Palawan, Philippines. Sabah, Malaysia: Asian Wetlands Symposium on seabird colony, evidently causing disturbance. Integrated Biodiversity Conservation: Linking Forests and Wetlands $e seabird population trends correlate well with the intensity 2011. of anthropogenic pressures. By 1998, when the no-visitor policy was Arquiza, Y. & White, A. T. (1999) Tales from Tubbataha: natural history, resource enforced, the Brown Booby population had declined by over 50% use, and conservation of Tubbataha Reefs, Palawan, Philippines. Second since the 1981 count by Kennedy (1982) and ‘lag e"ects’ probably edition. Makati, Philippines: Bookmark Inc. caused the decline to continue to 85% by 2002; since then there has Bibby, C. J., Burgess, N. D., Hill, D. A. & Mustoe, S. H. (2000). Bird census been a slow increase, although it is still about 43% lower than in techniques. Second edition. London: Academic Press. 1981. Today the park’s Bird and South Islets may be the only Sulu Bindoff, N. L., Willebrand, J., Artale, V., Cazenave, A., Gregory, J., Gulev, S., Sea islets which continue to be free of human-introduced predators Hanawa, K., Le Quéré, C., Levitus, S., Nojiri, Y., Shum, C. K., Talley, L. D. and from human disturbance (Jensen 2007). & Unnikrishnan, A. 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A rise in sea-level of this BirdLife International (2015) Species factsheet: Oceanodroma monorhis. magnitude would reduce the area of the islet from about 11,000 m% Downloaded from http://www.birdlife.org on 14/02/2015. to an estimated 5,000 m%, a major reduction in available breeding Carboneras, C., Christie, D. A., Jutglar, F., Garcia, E. F. J. & Kirwan, G. M. (2016) area, probably leading to a reduction in the population of Brown Red-footed Booby (Sula sula). In: J. del Hoyo, A. Elliott, J. Sargatal, Booby and ground-nesting tern species. D. A. Christie & E. de Juana, eds. Handbook of the birds of the world $e population dynamics of the seabirds of the Tubbataha Reefs alive. Barcelona: Lynx Edicions (retrieved from http://www.hbw.com/ is complex, and requires further research: there are no studies of the node/52624 on 4 April 2016). reproduction and survival rates of Philippine seabirds; dispersal of Carcallas, M. R. P. 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Appendix 1 Annotated list of the birds of Tubbataha Reefs Natural Park Key: † = new records for the Philippines, * = species not listed for Palawan province by Dickinson et al. (1991) or Kennedy et al. (2000). Area = location of records in Tubbataha Reefs Natural Park: B = Bird Islet, S = South Islet, RS = Ranger Station, A = Amos Rock, J = Jessie Beazley Reef, P = pelagic. Status in Philippines, based on Kennedy et al. (2000): M = Migrant, R = Resident. Occurrence in Philippines, based on Kennedy et al. (2000): Ex = Extirpated, Ra = Rare, LU = Locally Uncommon, U = Uncommon, LC = Locally Common, FC = Fairly Common, C = Common. No. = total number of birds seen.

Species Area Status Occ First record Subsequent records and years No. Notes * Northern Shoveler Spatula clypeata RS M U 26/10/2006 1 White-tailed Tropicbird Phaethon lepturus P M Ra 1/5/2006 1 Grey Nightjar Caprimulgus jotaka S M Ra 7/5/2007 1: 2008 2 Uniform Swiftlet Aerodramus vanikorensis J R C 1/5/2006 12 Edible-nest Swiftlet Aerodramus fuciphagus B R U 10/5/2013 1 Paci!c Swift Apus paci!cus B M, R U 5/5/2003 4 Oriental Cuckoo Cuculus saturatus B, S M U 6/5/2004 2: 2006, 2007 4 Brush Cuckoo Cacomantis variolosus B R C 26/10/1991 1 Red-legged Crake Rallina fasciata B, S R?, M? Ra 26/5/2002 2: 2010, 2012 3 Records include two found dead in May Slaty-legged Crake Rallina eurizonoides S R U 6/5/2004 1: 2008 3 All found dead in May * Barred Rail Hypotaenidia torquata B, S R C 5/5/2003 27 Breeding population in 2013: 2 * Bu"-banded Rail Hypotaenidia philippensis B R LC 14/5/2010 1 Slaty-breasted Rail Lewinia striata S R U 7/5/2004 1: 2013 3 White-breasted Waterhen Amaurornis phoenicurus B R C 5/5/2003 1 Baillon's Crake Zapornia pusilla B M U 9/5/2005 1 Watercock Gallicrex cinerea S R FC 8/5/2013 1 Common Moorhen Gallinula chloropus S M, R C 24/10/1991 1 † Swinhoe's Storm Petrel Hydrobates monorhis P M 11/5/2013 1 First country record (Jensen et al. 2015) Bulwer's Petrel Bulweria bulwerii P M Ra 1/5/2006 2: 2008, 2013 3 * Wedge-tailed Shearwater Ardenna paci!ca P M LU 24/10/1991 3: 2005, 2007, 2008 4 Yellow Bittern Ixobrychus sinensis B, S R C 26/10/1991 1: 2005 2 Cinnamon Bittern Ixobrychus cinnamomeus B, S R C 6/6/2002 1: 2002 3 Japanese Night Heron Gorsachius goisagi S M Ra 10/5/2005 1 Found dead. See species account * Black-crowned Night Heron Nycticorax nycticorax RS R LU 15/5/2010 1 Green-backed Heron Butorides striata B, S, RS M, R FC 6/5/2004 5: 2005–2007, 2012–2013 7 Cattle Egret Bubulcus alba B, S, RS M, R LC 26/10/1991 8: 2005–2006, 2009–2010, 2012–2013 23 Grey Heron Ardea cinerea B, S M U 26/5/2002 3: 2002, 2006 21 Great-billed Heron Ardea sumatrana S R LU 24/10/1991 1 Great White Egret Ardea albus B M, R U 26/10/1991 3: 2005, 2011, 2012 5 Intermediate Egret Ardea intermedia B M LC 26/10/1991 1: 2005 4 Little Egret Egretta garzetta B, S M, R C 26/10/1991 7: 2005–2007, 2011–2013 13 Chinese Egret Egretta eulophotes B, S, RS M Ra 23/3/1995 8: 2006–2012 21 Paci!c Reef Egret Egretta sacra B, S, RS R U 24/10/1991 Breeding population in 2013: 18 Great Frigatebird Fregata minor B, S, J M LU ? 21: 1995, 2001–2013 228 See species account Lesser Frigatebird Fregata ariel B, S, J M LU 24/10/1991 16: 2004–2013 63 * Christmas Frigatebird Fregata andrewsi B, S M Ra 5/5/2003 10: 2004–2009, 2011–2012 31 Jensen & Tan 2010 Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines 85

Species Area Status Occ First record Subsequent records and years No. Notes Masked Booby Sula dactylatra B R Ex? 29/6/1911 6: 1981, 1989, 1991, 1993, 1995 189 Last record 23 June 1995 Red-footed Booby Sula sula B, S, J R LC 15/6/1981 Breeding population in 2013: 3,568 Brown Booby Sula leucogaster B, S, J R Ra 29/6/1911 Breeding population in 2013: 2,155 Black-winged Stilt Himantopus himantopus RS M, R LC 4/2007 1 Paci!c Golden Plover Pluvialis fulva B M C 26/10/1991 2 Grey Plover Pluvialis squatarola B, RS M C 26/10/1991 6: 2005–2010, 2012 87 Kentish Plover Charadrius alexandrinus B M C 28/10/2006 1 Lesser Sand Plover Charadrius mongolus B, S, RS M C 24/10/1991 2: 1991, 2004 3 Greater Sand Plover Charadrius leschenaultii B M C 28/4/2006 5 Whimbrel Numenius phaeopus B, S, RS M C 24/10/1991 12: 1991, 1998, 2000, 2002, 2003, 2005, 2006, 2009 94 Eurasian Curlew Numenius arquata B M U 26/10/1991 4 * Black-tailed Godwit Limosa limosa B M Ra 26/10/1991 2: 2006, 2008 13 * Bar-tailed Godwit Limosa lapponica B M U 26/10/1991 1: 2008 4 * Red Knot Calidris canutus B M U 26/10/1991 1 * Sanderling Calidris alba B, S M U 29/4/2006 3: 2006, 2007, 2011 4 Red-necked Stint Calidris ru!collis B M C 26/10/1991 1 Ru" Calidris pugnax B M Ra 26/10/1991 2 Red-necked Phalarope Phalaropus lobatus B, RS, J M C 26/10/1991 5: 2004, 2005, 2008, 2009, 2011 49 Common Sandpiper Actitis hypoleucos S M C 8/5/2013 2 Common Greenshank Tringa nebularia B M C 26/10/1991 1: 2006 3 Green Sandpiper Tringa ochropus B M Ra 26/10/1991 2 Wood Sandpiper Tringa glareola B M C 28/10/2006 1: 2008 5 Grey-tailed Tattler Tringa brevipes B, S, RS M C 26/10/1991 17: 1991, 2004–2009, 2011–2013 502 Probably declining Ruddy Turnstone Arenaria interpres B, S, RS M FC 13–14/6/1981 25: 1991, 1995, 1997–2013 870 Probably declining Brown Noddy Anous stolidus B, S, J R LU 29/6/1911 Breeding population in 2013: 1,688 Black Noddy Anous minutus B, S, J R Ra 15/6/1981 Breeding population in 2013: 10,656 Bridled Tern Onychoprion anaethetus J, P M, R Ra 9/5/2009 2: 2010, 2013 10 Sooty Tern Onychoprion fuscatus B, S, J M, R Ra 13/6/1981 Breeding population in 2013: 3,771 Little Tern Sternula albifrons B, S, RS M, R U 22/3/1995 3: 2003, 2005, 2006 9 Whiskered Tern Chlidonias hybrida B, S, J M C 26/10/2006 4: 2011–2013 10 White-winged Tern Chlidonias leucopterus B, S, RS, J, P M FC 6/5/2004 14: 2005, 2006, 2009–2013 250 All but one record were of migrating #ocks Greater Crested Tern Thalasseus bergii B, S, RS, J R FC 29/6/1911 Breeding population in 2013: 10,500 Roseate Tern Sterna dougallii B, S, RS, A, J R? Ra 22/3/1995 5: 1995, 2004–2006, 2012 23 Black-naped Tern Sterna sumatrana B, RS, A, J R U 7/5/2004 10: 2005–2007, 2009–2011, 2013 37 Common Tern Sterna hirundo B, RS, J M U 6/5/2004 3: 2008, 2011, 2013 33 * Pomarine Skua Stercorarius pomarinus P M Ra 10/5/2005 Light phase adult Brown Boobook Ninox scutulata B, S M, R U 15/4/2004 4: 2004–2006, 2013 8 Migrant subspecies japonica Grey-faced Buzzard Butastur indicus B M FC 26/10/1991 1 * Blue-throated Bee-eater Merops viridis B R FC 9/5/2005 1 Ruddy King!sher Halcyon coromanda S M, R U 10/5/2005 1 Found dead * White-throated King!sher Halcyon gularis S R FC 30/4/2006 1 Found dead Collared King!sher Todiramphus chloris B, S R C 24/10/1991 13: 1991, 1993, 2000–2006, 2009 25 Two found dead Common King!sher Alcedo atthis B, S M C 24/10/1991 3: 1991, 2006 8 Oriental Hobby Falco severus S R U 6/5/2003 1 Peregrine Falcon Falco peregrinus B, S M U 7/5/2004 6: 2004–2007, 2011– 2013 8 All records were of migratory subspecies Western Hooded Pitta Pitta sordida S R C 26/5/2002 1 Found dead Brown Shrike Lanius cristatus B, S M C 24/10/1991 9: 1991, 2004, 2006, 2009, 2011, 2012 20 Large-billed Crow Corvus macrorhynchos S R C 30/4/2006 1 Found dead Barn Swallow Hirundo rustica B, S M C 24/10/1991 6: 1991, 2004, 2006 25 House Swallow Hirundo javanica B R C 28/10/2006 3 * Oriental Skylark Alauda gulgula RS R U 8/5/2005 1 Lanceolated Warbler Locustella lanceolata B, S M U 26/10/1991 2: 2007, 2013 3 Middendor"'s Grasshopper Warbler Locustella ochotensis S M U 10 /5/2005 1: 2006 2 Oriental Reed Warbler Acrocephalus orientalis B, S M C 24/10/1991 3: 1991, 2005, 2013 8 * Clamorous Reed Warbler Acrocephalus stentoreus S R U 10/5/2005 1 Arctic Warbler Phylloscopus borealis B, S, RS M C 15/10/1991 11: 2003–2006, 2009, 2011, 2012 22 Purple-backed Starling Agropsar sturninus B M 26/10/1991 2 Second country record (Jensen et al. 2015) Chestnut-cheeked Starling Agropsar philippensis B M U 28/10/2006 1: 2012 4 † Rosy Starling Pastor roseus S M 9/5/2009 1 First country record (Jensen et al. 2015) Blue Rock Thrush Monticola solitarius S M, R C 29/4/2006 1 Grey-streaked Flycatcher Muscicapa griseisticta B, S M C 26/10/1991 1: 2006 2 Narcissus Flycatcher Ficedula narcissina S M Ra 30/10/2006 1 Blue-and-white Flycatcher Cyanoptila cyanomelana B M Ra 26/10/1991 1 Eurasian Tree Sparrow Passer montanus B, S, R C 25/10/1991 Breeding population in 2013: 16 Forest Wagtail Dendronanthus indicus S M Ra 10/5/2005 1 White Wagtail Motacilla alba B, S M Ra 26/5/2002 1: 2009 2 Yellow Wagtail Motacilla "ava B, S, RS M C 6/5/2004 14: 2005–2006, 2009–2013 41 See species account Grey Wagtail Motacilla cinerea B, S, RS M C 26/10/1991 13: 2004 – 2006, 2009 – 2011, 2013 26 Olive-backed Pipit Anthus hodgsoni ? M U 9/5/2005 6: 2005, 2006, 2011 16 Pechora Pipit Anthus gustavi B, S M U 24/10/1991 6: 1991, 2004, 2005, 2008, 2009 8